Mechanical stretch: Physiological and pathological implications for human vascular endothelial cells

Vascular Cell

Volumn 7, Issue 1, 2015, Pages

  Jufri, Nurul F ^a   Mohamedali, Abidali ^a   Avolio, Alberto ^a   Baker, Mark S ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; REACTIVE OXYGEN METABOLITE; VASCULAR CELL ADHESION MOLECULE 1;

ANGIOGENESIS; APOPTOSIS; BLOOD VESSEL TONE; CELL FATE; CELL PROLIFERATION; CELL STRUCTURE; CELL SURFACE; CELL SURVIVAL; CELLULAR PARAMETERS; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HOMEOSTASIS; HUMAN; HUMAN CELL; HYPERTENSION; INFLAMMATION; INTRACELLULAR SIGNALING; MECHANICAL STRETCH; MECHANORECEPTOR; PRIORITY JOURNAL; REVIEW; VASCULAR ENDOTHELIAL CELL; VASCULAR HOMEOSTASIS;

EID: 84941790874     PISSN: None     EISSN: 2045824X     Source Type: Journal    
DOI: 10.1186/s13221-015-0033-z     Document Type: Review

References (102)

1. Li W, Sumpio BE. Strain-induced vascular endothelial cell proliferation requires PI3K-dependent mTOR-4E-BP1 signal pathway. Am J Physiol Heart Circ Physiol. 2005;288(4):1591-7. doi: 10.1152/ajpheart.00382.2004.
2. Joung IS, Iwamoto MN, Shiu YT, Quam CT. Cyclic strain modulates tubulogenesis of endothelial cells in a 3D tissue culture model. Microvasc Res. 2006;71(1):1-11. doi: 10.1016/j.mvr.2005.10.005.
3. Birukov KG. Cyclic stretch, reactive oxygen species, and vascular remodeling. Antioxid Redox Signal. 2009;11(7):1651-67. doi: 10.1089/ars.2008.2390.
4. Cheng TH, Shih NL, Chen SY, Loh SH, Cheng PY, Tsai CS, et al. Reactive oxygen species mediate cyclic strain-induced endothelin-1 gene expression via Ras/Raf/extracellular signal-regulated kinase pathway in endothelial cells. J Mol Cell Cardiol. 2001;33(10):1805-14. doi: 10.1006/jmcc.2001.1444.
5. Hu Z, Xiong Y, Han X, Geng C, Jiang B, Huo Y, et al. Acute mechanical stretch promotes eNOS activation in venous endothelial cells mainly via PKA and Akt pathways. PLoS One. 2013;8(8):e71359. doi: 10.1371/journal.pone.0071359.
6. Lehoux S, Castier Y, Tedgui A. Molecular mechanisms of the vascular responses to haemodynamic forces. J Intern Med. 2006;259(4):381-92. doi: 10.1111/j.1365-2796.2006.01624.x.
7. Lal H, Verma S, Golden H, Foster D, Holt A, Dostal D. Molecular signaling mechanisms of myocardial stretch: implications for heart disease. In: Kamkin A, Kiseleva I, editors. Mechanosensitivity of the heart. Mechanosensitivity in cells and tissues: Springer Netherlands. 2010. p. 55-81.
8. Anwar MA, Shalhoub J, Lim CS, Gohel MS, Davies AH. The effect of pressure-induced mechanical stretch on vascular wall differential gene expression. J Vasc Res. 2012;49(6):463-78. doi: 10.1159/000339151.
9. Chiu JJ, Usami S, Chien S. Vascular endothelial responses to altered shear stress: pathologic implications for atherosclerosis. Ann Med. 2009;41(1):19-28. doi: 10.1080/07853890802186921.
10. Ngai CY, Yao X. Vascular responses to shear stress: the involvement of mechanosensors in endothelial cells. Open Circ Vasc J. 2010;3:85-94.
11. Shyu KG. Cellular and molecular effects of mechanical stretch on vascular cells and cardiac myocytes. Clin Sci (Lond). 2009;116(5):377-89. doi: 10.1042/cs20080163.
12. Lacolley P. Mechanical influence of cyclic stretch on vascular endothelial cells. Cardiovasc Res. 2004;63(4):577-9. doi: 10.1016/j.cardiores.2004.06.017.
13. Thodeti CK, Matthews B, Ravi A, Mammoto A, Ghosh K, Bracha AL, et al. TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ Res. 2009;104(9):1123-30. doi: 10.1161/circresaha.108.192930.
14. Naruse K, Yamada T, Sokabe M. Involvement of SA channels in orienting response of cultured endothelial cells to cyclic stretch. Am J Physiol. 1998;274(5 Pt 2):H1532-8.
15. Adapala RK, Talasila PK, Bratz IN, Zhang DX, Suzuki M, Meszaros JG, et al. PKCalpha mediates acetylcholine-induced activation of TRPV4-dependent calcium influx in endothelial cells. Am J Physiol Heart Circ Physiol. 2011;301(3):H757-65. doi: 10.1152/ajpheart.00142.2011.
16. Berrout J, Jin M, O'Neil RG. Critical role of TRPP2 and TRPC1 channels in stretch-induced injury of blood-brain barrier endothelial cells. Brain Res. 2012;1436:1-12. doi: 10.1016/j.brainres.2011.11.044.
17. Suzuki M, Naruse K, Asano Y, Okamoto T, Nishikimi N, Sakurai T, et al. Up-regulation of integrin beta 3 expression by cyclic stretch in human umbilical endothelial cells. Biochem Biophys Res Commun. 1997;239(2):372-6. doi: 10.1006/bbrc.1997.7364.
18. Katsumi A, Naoe T, Matsushita T, Kaibuchi K, Schwartz MA. Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J Biol Chem. 2005;280(17):16546-9. doi: 10.1074/jbc.C400455200.
19. Zebda N, Dubrovskyi O, Birukov KG. Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvas Res. 2012;83(1):71-81. doi: 10.1016/j.mvr.2011.06.007.
20. Katanosaka Y, Bao JH, Komatsu T, Suemori T, Yamada A, Mohri S, et al. Analysis of cyclic-stretching responses using cell-adhesion-patterned cells. J Biotechnol. 2008;133(1):82-9. doi: 10.1016/j.jbiotec.2007.09.017.
21. Osawa M, Masuda M, Kusano K-i, Fujiwara K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J Cell Biol. 2002;158:773-85. doi: 10.1083/jcb.200205049.
22. Ikeda M, Kito H, Sumpio BE. Phosphatidylinositol-3 kinase dependent MAP kinase activation via p21ras in endothelial cells exposed to cyclic strain. Biochem Biophys Res Commun. 1999;257(3):668-71. doi: 10.1006/bbrc.1999.0532.
23. Shi F, Chiu YJ, Cho Y, Bullard TA, Sokabe M, Fujiwara K. Down-regulation of ERK but not MEK phosphorylation in cultured endothelial cells by repeated changes in cyclic stretch. Cardiovas Res. 2007;73(4):813-22. doi: 10.1016/j.cardiores.2006.12.014.
24. Fujiwara K. Mechanical stresses keep endothelial cells healthy: beneficial effects of a physiological level of cyclic stretch on endothelial barrier function. Am J Physiol Lung Cell M Physiol. 2003;285(4):L782-4. doi: 10.1152/ajplung.00142.2003.
25. Ueki Y, Sakamoto N, Ohashi T, Sato M. Morphological responses of vascular endothelial cells induced by local stretch transmitted through intercellular junctions. Exp Mech. 2009;49(1):125-34. doi: 10.1007/s11340-008-9143-3.
26. Tojkander S, Gateva G, Lappalainen P. Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci. 2012;125(Pt 8):1855-64. doi: 10.1242/jcs.098087.
27. Takemasa T, Yamaguchi T, Yamamoto Y, Sugimoto K, Yamashita K. Oblique alignment of stress fibers in cells reduces the mechanical stress in cyclically deforming fields. Eur J Cell Biol. 1998;77(2):91-9. doi: 10.1016/s0171-9335(98)80076-9.
28. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC. Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J C Biol. 2005;171(2):209-15. doi: 10.1083/jcb.200505018.
29. Yoshigi M, Clark EB, Yost HJ. Quantification of stretch-induced cytoskeletal remodeling in vascular endothelial cells by image processing. Cytometry A. 2003;55(2):109-18. doi: 10.1002/cyto.a.10076.
30. Huang W, Sakamoto N, Miyazawa R, Sato M. Role of paxillin in the early phase of orientation of the vascular endothelial cells exposed to cyclic stretching. Biochem Biophys Res Commun. 2012;418(4):708-13. doi: 10.1016/j.bbrc.2012.01.083.
31. Moretti M, Prina-Mello A, Reid AJ, Barron V, Prendergast PJ. Endothelial cell alignment on cyclically-stretched silicone surfaces. J Mater Sci Mater Med. 2004;15(10):1159-64. doi: 10.1023/b:jmsm.0000046400.18607.72.
32. Barron V, Brougham C, Coghlan K, McLucas E, O'Mahoney D, Stenson-Cox C, et al. The effect of physiological cyclic stretch on the cell morphology, cell orientation and protein expression of endothelial cells. J Mater Sci Mater Med. 2007;18(10):1973-81. doi: 10.1007/s10856-007-3125-3.
33. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol. 2007;292(3):H1209-24. doi: 10.1152/ajpheart.01047.2006.
34. Wang JH, Goldschmidt-Clermont P, Wille J, Yin FC. Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J Biomech. 2001;34(12):1563-72.
35. Kaunas R, Nguyen P, Usami S, Chien S. Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proc Natl Acad Sci U S A. 2005;102(44):15895-900. doi: 10.1073/pnas.0506041102.
36. Kaunas R, Usami S, Chien S. Regulation of stretch-induced JNK activation by stress fiber orientation. Cell Signal. 2006;18(11):1924-31. doi: 10.1016/j.cellsig.2006.02.008.
37. Hsu HJ, Lee CF, Locke A, Vanderzyl SQ, Kaunas R. Stretch-induced stress fiber remodeling and the activations of JNK and ERK depend on mechanical strain rate, but not FAK. PLoS One. 2010;5(8):e12470. doi: 10.1371/journal.pone.0012470.
38. Luo SS, Sugimoto K, Fujii S, Takemasa T, Fu SB, Yamashita K. Role of heat shock protein 70 in induction of stress fiber formation in rat arterial endothelial cells in response to stretch stress. Acta Histochem Cytochem. 2007;40(1):9-17. doi: 10.1267/ahc.06011.
39. Wang JH, Thampatty BP. An introductory review of cell mechanobiology. Biomech Model Mechanobiol. 2006;5(1):1-16. doi: 10.1007/s10237-005-0012-z.
40. Mekkawy AH, Pourgholami MH, Morris DL. Involvement of urokinase-type plasminogen activator system in cancer: an overview. Med Res Rev. 2014;34(5):918-56. doi: 10.1002/med.21308.
41. Loftus IM, Thompson MM. The role of matrix metalloproteinases in vascular disease. Vasc Med. 2002;7(2):117-33. doi: 10.1191/1358863x02vm420ra
42. Rundhaug JE. Matrix metalloproteinases and angiogenesis. J Cell Mol Med. 2005;9(2):267-85.
43. von Offenberg SN, Cummins PM, Birney YA, Cullen JP, Redmond EM, Cahill PA. Cyclic strain-mediated regulation of endothelial matrix metalloproteinase-2 expression and activity. Cardiovasc Res. 2004;63(4):625-34. doi: 10.1016/j.cardiores.2004.05.008.
44. Wang B-W, Chang H, Lin S, Kuan P, Shyu K-G. Induction of matrix metalloproteinases-14 and -2 by cyclical mechanical stretch is mediated by tumor necrosis factor-alpha in cultured human umbilical vein endothelial cells. Cardiovasc Res. 2003;59:460-9.
45. Liu X-m L, Ensenat D, Wang H, Schafer AI, Durante W. Physiologic cyclic stretch inhibits apoptosis in vascular endothelium. FEBS Lett. 2003;541:52-6. doi: 10.1016/S0014-5793(03)00285-0.
46. Agewall S. Matrix metalloproteinases and cardiovascular disease. Eur Heart J. 2006;27:121-2. doi: 10.1093/eurheartj/ehi639.
47. Zheng W, Christensen LP, Tomanek RJ. Stretch induces upregulation of key tyrosine kinase receptors in microvascular endothelial cells. Am J Physiol Heart Circl Physiol. 2004;52242:2739-45. doi: 10.1152/ajpheart.00410.2004.
48. Zheng W, Christensen LP, Tomanek RJ. Differential effects of cyclic and static stretch on coronary microvascular endothelial cell receptors and vasculogenic / angiogenic responses. Am J Physiol Heart Circl Physiol. 2008;52242:794-800. doi: 10.1152/ajpheart.00343.2008.
49. Bocci G, Fasciani A, Danesi R, Viacava P, Genazzani AR, Del Tacca M. In-vitro evidence of autocrine secretion of vascular endothelial growth factor by endothelial cells from human placental blood vessels. Mol Hum Reprod. 2001;7(8):771-7.
50. Wang C, Jiao C, Hanlon HD, Zheng W, Tomanek RJ, Schatteman GC. Mechanical, cellular, and molecular factors interact to modulate circulating endothelial cell progenitors. Am J Physiol Heart Circl Physiol. 2004;286(5):H1985-93. doi: 10.1152/ajpheart.00431.2003.
51. Zheng W, Seftor EA, Meininger CJ, Hendrix MJ, Tomanek RJ. Mechanisms of coronary angiogenesis in response to stretch: role of VEGF and TGF-beta. Am J Physiol Heart Circl Physiol. 2001;280(2):H909-17.
52. Wilkins JR, Pike DB, Gibson CC, Kubota A, Shiu YT. Differential effects of cyclic stretch on bFGF- and VEGF-induced sprouting angiogenesis. Biotechnol Prog. 2014;30(4):879-88. doi: 10.1002/btpr.1883.
53. Bao P, Kodra A, Tomic-Canic M, Golinko MS, Ehrlich HP, Brem H. The role of vascular endothelial growth factor in wound healing. J Surg Res. 2009;153(2):347-58. doi: 10.1016/j.jss.2008.04.023.
54. Yung YC, Chae J, Buehler MJ, Hunter CP, Mooney DJ. Cyclic tensile strain triggers a sequence of autocrine and paracrine signaling to regulate angiogenic sprouting in human vascular cells. Proc Natl Acad Sci U S A. 2009;106:15279-84. doi: 10.1073/pnas.0905891106.
55. Von Offenberg SN, Cummins PM, Cotter EJ, Fitzpatrick PA, Birney YA, Redmond EM, et al. Cyclic strain-mediated regulation of vascular endothelial cell migration and tube formation. Biochem Biophys Res Commun. 2005;329(2):573-82. doi: 10.1016/j.bbrc.2005.02.013.
56. Liu WF, Nelson CM, Tan JL, Chen CS. Cadherins, RhoA, and Rac1 are differentially required for stretch-mediated proliferation in endothelial versus smooth muscle cells. Circ Res. 2007;101:44-52. doi: 10.1161/CIRCRESAHA.107.158329.
57. Hurley NE, Schildmeyer LA, Bosworth KA, Sakurai Y, Eskin SG, Hurley LH, et al. Modulating the functional contributions of c-Myc to the human endothelial cell cyclic strain response. J Vasc Res. 2010;47:80-90. doi: 10.1159/000235928.
58. Zhang K, Cao J, Dong R, Du J. Early growth response protein 1 promotes restenosis by upregulating intercellular adhesion molecule-1 in vein graft. Oxid Med Cell Longev. 2013;2013:1-9. doi: 10.1155/2013/432409.
59. Michaelis UR, Fleming I. From endothelium-derived hyperpolarizing factor (EDHF) to angiogenesis: Epoxyeicosatrienoic acids (EETs) and cell signaling. Pharmacol Ther. 2006;111(3):584-95. doi: 10.1016/j.pharmthera.2005.11.003.
60. Cifarelli V, Lee S, Kim DH, Zhang T, Kamagate A, Slusher S, et al. FOXO1 mediates the autocrine effect of endothelin-1 on endothelial cell survival. Mol Endocrinol. 2012;26(7):1213-24. doi: 10.1210/me.2011-1276.
61. Thacher TN, Silacci P, Stergiopulos N, da Silva RF. Autonomous effects of shear stress and cyclic circumferential stretch regarding endothelial dysfunction and oxidative stress: an ex vivo arterial model. J Vasc Res. 2010;47(4):336-45. doi: 10.1159/000265567.
62. Takeda H, Komori K, Nishikimi N, Nimura Y, Sokabe M, Naruse K. Bi-phasic activation of eNOS in response to uni-axial cyclic stretch is mediated by differential mechanisms in BAECs. Life Sci. 2006;79(3):233-9. doi: 10.1016/j.lfs.2005.12.051.
63. Fisslthaler B, Popp R, Michaelis UR, Kiss L, Fleming I, Busse R. Cyclic stretch enhances the expression and activity of coronary endothelium-derived hyperpolarizing factor synthase. Hypertension. 2001;38(6):1427-32. doi: 10.1161/hy1201.096532.
64. Toda M, Yamamoto K, Shimizu N, Obi S, Kumagaya S, Igarashi T, et al. Differential gene responses in endothelial cells exposed to a combination of shear stress and cyclic stretch. J Biotechnol. 2008;133:239-44. doi: 10.1016/j.jbiotec.2007.08.009.
65. Koller A. Signaling pathways of mechanotransduction in arteriolar endothelium and smooth muscle cells in hypertension. Microcirculation. 2002;9:277-94. doi: 10.1038/sj.mn/7800142.
66. Ali MH, Mungai PT, Schumacker PT, Mir H, Stretch- PTS. Stretch-induced phosphorylation of focal adhesion kinase in endothelial cells: role of mitochondrial oxidants. Am J Physiol Heart Circl Physiol. 2006;60611:38-45. doi: 10.1152/ajplung.00287.2004.
67. Goettsch C, Goettsch W, Arsov A, Hofbauer LC, Bornstein SR, Morawietz H. Long-term cyclic strain downregulates endothelial Nox4. Antioxid Redox Signal. 2009;11:2385-97. doi: 10.1089/ARS.2009.2561.
68. Ali MH, Pearlstein DP, Mathieu CE, Schumacker PT. Mitochondrial requirement for endothelial responses to cyclic strain: implications for mechanotransduction. Am J Physiol Lung Cell Mol Physiol. 2004;287:486-96. doi: 10.1152/ajplung.00389.2003.
69. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340:115-26.
70. Spescha RD, Glanzmann M, Simic B, Witassek F, Keller S, Akhmedov A, et al. Adaptor protein p66Shc mediates hypertension-associated, cyclic stretch-dependent, endothelial damage. Hypertension. 2014;64:347-53. doi: 10.1161/HYPERTENSIONAHA.113.02129.
71. Wagner AH, Kautz O, Fricke K, Zerr-Fouineau M, Demicheva E, Güldenzoph B, et al. Upregulation of glutathione peroxidase offsets stretch-induced proatherogenic gene expression in human endothelial cells. Arterioscler Thromb Vasc Biol. 2009;29:1894-901. doi: 10.1161/ATVBAHA.109.194738.
72. Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev. 2009;89(2):481-534. doi: 10.1152/physrev.00042.2007.
73. Frye SR, Yee A, Eskin SG, Guerra R, Cong X, McIntire LV. cDNA microarray analysis of endothelial cells subjected to cyclic mechanical strain: importance of motion control. Physiol Genomics. 2005;21(1):124-30. doi: 10.1152/physiolgenomics.00029.2003.
74. Xiong Y, Hu Z, Han X, Jiang B, Zhang R, Zhang X, et al. Hypertensive stretch regulates endothelial exocytosis of Weibel-Palade bodies through VEGF receptor 2 signaling pathways. Cell Res. 2013;23:820-34. doi: 10.1038/cr.2013.56.
75. Kobayashi S, Nagino M, Komatsu S, Naruse K, Nimura Y, Nakanishi M, et al. Stretch-induced IL-6 secretion from endothelial cells requires NF-κB activation. Biochem Biophys Res Commun. 2003;308:306-12. doi: 10.1016/S0006-291X(03)01362-7.
76. Korff T, Aufgebauer K, Hecker M. Cyclic stretch controls the expression of CD40 in endothelial cells by changing their transforming growth factor-beta1 response. Circulation. 2007;116:2288-97. doi: 10.1161/CIRCULATIONAHA.107.730309.
77. Kou B, Zhang J, Singer DRJ. Effects of cyclic strain on endothelial cell apoptosis and tubulogenesis are dependent on ROS production via NAD(P)H subunit p22phox. Microvasc Res. 2009;77:125-33. doi: 10.1016/j.mvr.2008.08.001.
78. Nishimura K, Li W, Hoshino Y, Kadohama T, Asada H, Ohgi S, et al. Role of AKT in cyclic strain-induced endothelial cell proliferation and survival. Am J Physiol Cell Physiol. 2006;8062:812-21. doi: 10.1152/ajpcell.00347.2005.
79. Lemarie CA, Tharaux PL, Lehoux S. Extracellular matrix alterations in hypertensive vascular remodeling. J Mol Cell Cardiol. 2010;48(3):433-9. doi: 10.1016/j.yjmcc.2009.09.018.
80. Okada M, Matsumori A, Ono K, Furukawa Y, Shioi T, Iwasaki A, et al. Cyclic stretch upregulates production of interleukin-8 and monocyte chemotactic and activating factor/monocyte chemoattractant protein-1 in human endothelial cells. Arterioscler Thromb Vasc Biol. 1998;18(6):894-901. doi: 10.1161/01.ATV.18.6.894
81. Lee YU, Hayman D, Sprague EA, Han HC. Effects of axial stretch on cell proliferation and intimal thickness in arteries in organ culture. Cell Mol Bioeng. 2010;3(3):286-95. doi: 10.1007/s12195-010-0128-9.
82. Hatami J, Tafazzoli-Shadpour M, Haghighipour N, Shokrgozar MA, Janmaleki M. Influence of cyclic stretch on mechanical properties of endothelial cells. Exp Mech. 2013;53(8):1291-8. doi: 10.1007/s11340-013-9744-3.
83. Cevallos M, Riha GM, Wang X, Yang H, Yan S, Li M, et al. Cyclic strain induces expression of specific smooth muscle cell markers in human endothelial cells. Differentiation. 2006;74(9-10):552-61. doi: 10.1111/j.1432-0436.2006.00089.x.
84. Shoajei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N. Alteration of human umbilical vein endothelial cell gene expression in different biomechanical environments. Cell Biol Int. 2014;38(5):577-81. doi: 10.1002/cbin.10237.
85. Montezano AC, Touyz RM. Reactive oxygen species and endothelial function-role of nitric oxide synthase uncoupling and Nox family nicotinamide adenine dinucleotide phosphate oxidases. Basic Clin Pharmacol Toxicol. 2012;110(1):87-94. doi: 10.1111/j.1742-7843.2011.00785.x.
86. Dangas G. Restenosis: repeat narrowing of a coronary artery: prevention and treatment. Circulation. 2002;105(22):2586-87. doi: 10.1161/01.CIR.0000019122.00032.DF.
87. Stula M, Orzechowski HD, Gschwend S, Vetter R, von Harsdorf R, Dietz R, et al. Influence of sustained mechanical stress on Egr-1 mRNA expression in cultured human endothelial cells. Mol Cell Biochem. 2000;210(1-2):101-8.
88. Juvela S. Prevalence of and risk factors for intracranial aneurysms. Lancet Neurol. 2011;10(7):595-7. doi: 10.1016/s1474-4422(11)70125-9.
89. Rinkel GJ, Djibuti M, Algra A, van Gijn J. Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke. 1998;29(1):251-6. doi: 10.1161/01.STR.29.1.251.
90. Linn FH, Rinkel GJ, Algra A, van Gijn J. Incidence of subarachnoid hemorrhage: role of region, year, and rate of computed tomography: a meta-analysis. Stroke. 1996;27(4):625-9.
91. Fox B, Humphries WE, Doss VT, Hoit D, Elijovich L, Arthur AS. Rupture of giant vertebrobasilar aneurysm following flow diversion: mechanical stretch as a potential mechanism for early aneurysm rupture. J Neurointerv Surg. 2014;00:1-4. doi: 10.1136/bcr-2014-011325.
92. Shikata Y, Rios A, Kawkitinarong K, DePaola N, Garcia JG, Birukov KG. Differential effects of shear stress and cyclic stretch on focal adhesion remodeling, site-specific FAK phosphorylation, and small GTPases in human lung endothelial cells. Exp Cell Res. 2005;304(1):40-9. doi: 10.1016/j.yexcr.2004.11.001.
93. Owatverot TB, Oswald SJ, Chen Y, Wille JJ, Yin FC. Effect of combined cyclic stretch and fluid shear stress on endothelial cell morphological responses. J Biomech Eng. 2005;127(3):374-82. doi: 10.1115/1.1894180.
94. Haghighipour N, Tafazzoli-Shadpour M, Shokrgozar MA, Amini S. Effects of cyclic stretch waveform on endothelial cell morphology using fractal analysis. Artif Organs. 2010;34(6):481-90. doi: 10.1111/j.1525-1594.2010.01003.x.
95. Wang J, Lu D, Mao D, Long M. Mechanomics: an emerging field between biology and biomechanics. Protein Cell. 2014;5(7):518-31. doi: 10.1007/s13238-014-0057-9.
96. 2+ rather than of cAMP. Life Sci. 2000;67:2605-13.
97. Naruse K, Sai X, Yokoyama N, Sokabe M. Uni-axial cyclic stretch induces c-src activation and translocation in human endothelial cells via SA channel activation. FEBS Lett. 1998;441:111-5.
98. Naruse K, Yamada T, Sai X, Hamaguchi M, Sokabe M. Pp125 FAK is required for stretch dependent morphological response of endothelial cells. Oncogene. 1998;17:455-63.
99. Shukla a, Dunn aR, Moses Ma, Van Vliet KJ. Endothelial cells as mechanical transducers: enzymatic activity and network formation under cyclic strain. Mech Chem Biosyst. 2004;1:279-90.
100. Demicheva E, Hecker M, Korff T. Stretch-induced activation of the transcription factor activator protein-1 controls monocyte chemoattractant protein-1 expression during arteriogenesis. Circ Res. 2008;103:477-84. doi: 10.1161/CIRCRESAHA.108.177782.
101. Zhao H, Hiroi T, Hansen BS, Rade JJ. Cyclic stretch induces cyclooxygenase-2 gene expression in vascular endothelial cells via activation of nuclear factor kappa-beta. Biochem Biophys Res Commun. 2009;389:599-601. doi: 10.1016/j.bbrc.2009.09.028.
102. Wung BS, Cheng JJ, Shyue S-K, Wang DL. NO modulates monocyte chemotactic protein-1 expression in endothelial cells under cyclic strain. Arterioscler Thromb Vasc Biol. 2001;21:1941-47. doi: 10.1161/hq1201.099428.